Article | Published:

Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation

Nature Ecology & Evolutionvolume 2pages11281138 (2018) | Download Citation


A substantial part of biodiversity is thought to have arisen from adaptive radiations in which one lineage rapidly diversified into multiple lineages specialized to many different niches. However, selection and drift reduce genetic variation during adaptation to new niches and may thus prevent or slow down further niche shifts. We tested whether rapid adaptation is still possible from a highly derived ecotype in the adaptive radiation of threespine stickleback on the Haida Gwaii archipelago, Western Canada. In a 19-year selection experiment, we let giant sticklebacks from a large blackwater lake evolve in a small clearwater pond without vertebrate predators. A total of 56 whole genomes from the experiment and 26 natural populations revealed that adaptive genomic change was rapid in many small genomic regions and encompassed 75% of the change between 12,000-year-old ecotypes. Genomic change was as fast as phenotypic change in defence and trophic morphology, and both were largely parallel between the short-term selection experiment and long-term natural adaptive radiation. Our results show that functionally relevant standing genetic variation can persist in derived radiation members, allowing adaptive radiations to unfold very rapidly.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000).

  2. 2.

    Grant, P. R. Speciation and the adaptive radiation of Darwin finches. Am. Sci. 69, 653–663 (1981).

  3. 3.

    Losos, J. B., Jackman, T. R., Larson, A., Queiroz, K. & Rodriguez-Schettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998).

  4. 4.

    West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, Oxford, 2003).

  5. 5.

    Muschick, M., Barluenga, M., Salzburger, W. & Meyer, A. Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol. Biol. 11, 116 (2011).

  6. 6.

    Barrett, R. D. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).

  7. 7.

    Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).

  8. 8.

    Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).

  9. 9.

    Meier, J. I. et al. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8, 14363 (2017).

  10. 10.

    Price, T. D., Qvarnstrom, A. & Irwin, D. E. The role of phenotypic plasticity in driving genetic evolution. Proc. Biol. Sci. 270, 1433–1440 (2003).

  11. 11.

    Schlotterer, C., Kofler, R., Versace, E., Tobler, R. & Franssen, S. U. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity (Edinb.) 116, 248 (2016).

  12. 12.

    Barrett, S. C. H., Colautti, R. I., Dlugosch, K. M. & Rieseberg, L. H. Invasion Genetics: The Baker and Stebbins Legacy (Wiley-Blackwell, Hoboken, NJ, 2016).

  13. 13.

    Burke, M. K. et al. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587–590 (2010).

  14. 14.

    Fritz, M. L. et al. Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices. Mol. Ecol. 27, 167–181 (2018).

  15. 15.

    Tobler, R. et al. Massive habitat-specific genomic response in D. melanogaster populations during experimental evolution in hot and cold environments. Mol. Biol. Evol. 31, 364–375 (2014).

  16. 16.

    Graves, J. L. et al. Genomics of parallel experimental evolution in Drosophila. Mol. Biol. Evol. 34, 831–842 (2017).

  17. 17.

    Huang, Y., Wright, S. I. & Agrawal, A. F. Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet. 10, e1004527 (2014).

  18. 18.

    Franks, S. J., Kane, N. C., O’Hara, N. B., Tittes, S. & Rest, J. S. Rapid genome-wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools. Mol. Ecol. 25, 3622–3631 (2016).

  19. 19.

    van’t Hof, A. E., Edmonds, N., Dalikova, M., Marec, F. & Saccheri, I. J. Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332, 958–960 (2011).

  20. 20.

    Reid, N. M. et al. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354, 1305–1308 (2016).

  21. 21.

    Fraser, B. A., Kunstner, A., Reznick, D. N., Dreyer, C. & Weigel, D. Population genomics of natural and experimental populations of guppies (Poecilia reticulata). Mol. Ecol. 24, 389–408 (2015).

  22. 22.

    Hendry, A. P. & Kinnison, M. T. Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53, 1637–1653 (1999).

  23. 23.

    Reznick, D. N. & Ghalambor, C. K. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112-113, 183–198 (2001).

  24. 24.

    Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 18, 94–101 (2003).

  25. 25.

    Bell, M. A., Aguirre, W. E. & Buck, N. J. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58, 814–824 (2004).

  26. 26.

    Terekhanova, N. V. et al. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 10, e1004696 (2014).

  27. 27.

    Lescak, E. A. et al. Evolution of stickleback in 50 years on earthquake-uplifted islands. Proc. Natl Acad. Sci. USA 112, E7204–E7212 (2015).

  28. 28.

    Aguirre, W. E. & Bell, M. A. Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol. J. Linn. Soc. 105, 817–831 (2012).

  29. 29.

    Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862 (2010).

  30. 30.

    Reimchen, T. E., Bergstrom, C. & Nosil, P. Natural selection and the adaptive radiation of Haida Gwaii stickleback. Evol. Ecol. Res. 15, 241–269 (2013).

  31. 31.

    Moodie, G. E. E. & Reimchen, T. E. Phenetic variation and habitat differences in Gasterosteus populations of the Queen Charlotte Islands. Syst. Zool. 25, 49–61 (1976).

  32. 32.

    Reimchen, T. E. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 240–276 (Oxford Univ. Press, Oxford, 1994).

  33. 33.

    Bergstrom, C. A. & Reimchen, T. E. Habitat dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations. J. Evol. Biol. 18, 939–948 (2005).

  34. 34.

    Deagle, B. E., Jones, F. C., Absher, D. M., Kingsley, D. M. & Reimchen, T. E. Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide single nucleotide polymorphism genotyping. Mol. Ecol. 22, 1917–1932 (2013).

  35. 35.

    Reimchen, T. E. Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: functional implications for the ancestral plate condition. Behaviour 137, 1081–1096 (2000).

  36. 36.

    Reimchen, T. E. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus—an adaptation to predators. Can. J. Zool. 58, 1232–1244 (1980).

  37. 37.

    Reimchen, T. E. & Nosil, P. Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56, 2472–2483 (2002).

  38. 38.

    Reimchen, T. E. & Nosil, P. Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58, 1274–1281 (2004).

  39. 39.

    Reimchen, T. E., Stinson, E. M. & Nelson, J. S. Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands. Can. J. Zool. 63, 2944–2951 (1985).

  40. 40.

    Spoljaric, M. A. & Reimchen, T. E. 10 000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J. Fish. Biol. 70, 1484–1503 (2007).

  41. 41.

    Leaver, S. D. & Reimchen, T. E. Abrupt changes in defence and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol. J. Linn. Soc. 107, 494–509 (2012).

  42. 42.

    Moodie, G. E. E. Morphology, life-history, and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada. Can. J. Zool. 50, 721–732 (1972).

  43. 43.

    Moodie, G. E. E. Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28, 155–167 (1972).

  44. 44.

    Oreilly, P., Reimchen, T. E., Beech, R. & Strobeck, C. Mitochondrial DNA in Gasterosteus and pleistocene glacial refugium on the Queen Charlotte Islands, British Columbia. Evolution 47, 678–684 (1993).

  45. 45.

    Flamarique, I. N., Bergstrom, C., Cheng, C. L. & Reimchen, T. E. Role of the iridescent eye in stickleback female mate choice. J. Exp. Biol. 216, 2806–2812 (2013).

  46. 46.

    Deagle, B. E. et al. Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions. Proc. Biol. Sci. 279, 1277–1286 (2012).

  47. 47.

    Peichel, C. L. & Marques, D. A. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Phil. Trans. R. Soc. Lond. B 372, 20150486 (2017).

  48. 48.

    Peichel, C. L. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001).

  49. 49.

    Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).

  50. 50.

    Colosimo, P. F. et al. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2, E109 (2004).

  51. 51.

    Wark, A. R. et al. Genetic architecture of variation in the lateral line sensory system of threespine sticklebacks. G3 2, 1047–1056 (2012).

  52. 52.

    Greenwood, A. K., Wark, A. R., Yoshida, K. & Peichel, C. L. Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr. Biol. 23, 1884–1888 (2013).

  53. 53.

    Rennison, D. J., Owens, G. L., Heckman, N., Schluter, D. & Veen, T. Rapid adaptive evolution of colour vision in the threespine stickleback radiation. Proc. Biol. Sci. 283, 20160242 (2016).

  54. 54.

    Perez-Leighton, C. E., Schmidt, T. M., Abramowitz, J., Birnbaumer, L. & Kofuji, P. Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur. J. Neurosci. 33, 856–867 (2011).

  55. 55.

    Nakajima, Y., Moriyama, M., Hattori, M., Minato, N. & Nakanishi, S. Isolation of ON bipolar cell genes via hrGFP-coupled cell enrichment using the mGluR6 promoter. J. Biochem. 145, 811–818 (2009).

  56. 56.

    Amsterdam, A. et al. Identification of 315 genes essential for early zebrafish development. Proc. Natl Acad. Sci. USA 101, 12792–12797 (2004).

  57. 57.

    Nuckels, R. J., Ng, A., Darland, T. & Gross, J. M. The vacuolar-ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Invest. Ophthalmol. Vis. Sci. 50, 893–905 (2009).

  58. 58.

    Howe, D. G. et al. ZFIN, the zebrafish model organism database: increased support for mutants and transgenics. Nucleic Acids Res. 41, D854–D860 (2013).

  59. 59.

    Marques, D. A. et al. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLoS Biol. 15, e2001627 (2017).

  60. 60.

    Gwynn, B., Smith, R. S., Rowe, L. B., Taylor, B. A. & Peters, L. L. A mouse TRAPP-related protein is involved in pigmentation. Genomics 88, 196–203 (2006).

  61. 61.

    Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101–104 (2006).

  62. 62.

    Dickinson, M. E. et al. High-throughput discovery of novel developmental phenotypes. Nature 537, 508–514 (2016).

  63. 63.

    Ignatius, M. S., Moose, H. E., El-Hodiri, H. M. & Henion, P. D. colgate/hdac1 repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev. Biol. 313, 568–583 (2008).

  64. 64.

    Patterson, L. B. & Parichy, D. M. Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet. 9, e1003561 (2013).

  65. 65.

    Miller, C. T. et al. cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131, 1179–1189 (2007).

  66. 66.

    Rosenblum, E. B., Hoekstra, H. E. & Nachman, M. W. Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution 58, 1794–1808 (2004).

  67. 67.

    Malek, T. B., Boughman, J. W., Dworkin, I. & Peichel, C. L. Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback. Mol. Ecol. 21, 5265–5279 (2012).

  68. 68.

    Miller, C. T. et al. Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197, 405–420 (2014).

  69. 69.

    Lamichhaney, S. et al. A beak size locus in Darwin’s finches facilitated character displacement during a drought. Science 352, 470–474 (2016).

  70. 70.

    Gingerich, P. D. Rates of evolution: effects of time and temporal scaling. Science 222, 159–161 (1983).

  71. 71.

    Rennison, D. J., Owens, G. L. & Taylor, J. S. Opsin gene duplication and divergence in ray-finned fish. Mol. Phylogenet. Evol. 62, 986–1008 (2012).

  72. 72.

    Reimchen, T. E. Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus. Behaviour 132, 1079–1094 (1995).

  73. 73.

    Stinson, E. M. Threespine Sticklebacks (Gasterosteus aculeatus) in Drizzle Lake and Its Inlet, Queen Charlotte Islands: Ecological and Behavioural Relationships and Their Relevance to Reproductive Isolation. MSc thesis, Univ. Alberta (1983).

  74. 74.

    Dlugosch, K. M. & Parker, I. M. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431–449 (2008).

  75. 75.

    Keller, I. et al. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol. Ecol. 22, 2848–2863 (2013).

  76. 76.

    McGee, M. D., Neches, R. Y. & Seehausen, O. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25, 260–268 (2016).

  77. 77.

    Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).

  78. 78.

    Dasmahapatra, K. K. et al. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).

  79. 79.

    Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).

  80. 80.

    Glazer, A. M., Killingbeck, E. E., Mitros, T., Rokhsar, D. S. & Miller, C. T. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3 5, 1463–1472 (2015).

  81. 81.

    Delaneau, O., Howie, B., Cox, A. J., Zagury, J. F. & Marchini, J. Haplotype estimation using sequencing reads. Am. J. Hum. Genet. 93, 687–696 (2013).

  82. 82.

    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).

  83. 83.

    Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y. & Wang, J. SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS ONE 7, e37558 (2012).

  84. 84.

    Fumagalli, M. et al. Quantifying population genetic differentiation from next-generation sequencing data. Genetics 195, 979–992 (2013).

  85. 85.

    McLaren, W. et al. The Ensembl Variant Effect Predictor. Genome Biol. 17, 122 (2016).

  86. 86.

    Picard Tools (Broad Institute, 2017);

  87. 87.

    Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strainw1118; iso-2; iso-3. Fly (Austin) 6, 80–92 (2012).

  88. 88.

    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

  89. 89.

    Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).

  90. 90.

    Willing, E. M., Dreyer, C. & van Oosterhout, C. Estimates of genetic differentiation measured by F ST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7, e42649 (2012).

  91. 91.

    Bhatia, G., Patterson, N., Sankararaman, S. & Price, A. L. Estimating and interpreting F ST: the impact of rare variants. Genome Res. 23, 1514–1521 (2013).

  92. 92.

    Excoffier, L., Dupanloup, I., Huerta-Sanchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).

  93. 93.

    Feulner, P. G. et al. Genomics of divergence along a continuum of parapatric population differentiation. PLoS Genet. 11, e1004966 (2015).

  94. 94.

    Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).

  95. 95.

    Garud, N. R., Messer, P. W., Buzbas, E. O. & Petrov, D. A. Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps. PLoS Genet. 11, e1005004 (2015).

  96. 96.

    Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, U913–U918 (2007).

  97. 97.

    Szpiech, Z. A. & Hernandez, R. D. selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol. Biol. Evol. 31, 2824–2827 (2014).

  98. 98.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016);

  99. 99.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

  100. 100.

    Gillespie, J. H. Population Genetics: A Concise Guide 2nd edn (Johns Hopkins Univ. Press, Baltimore, MA, 2004).

  101. 101.

    Szklarczyk, D. et al. STRINGv10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).

  102. 102.

    Blake, J. A. et al. Mouse Genome Database (MGD)-2017: community knowledge resource for the laboratory mouse. Nucleic Acids Res. 45, D723–D729 (2017).

  103. 103.

    Shimoyama, M. et al. The Rat Genome Database 2015: genomic, phenotypic and environmental variations and disease. Nucleic Acids Res. 43, D743–D750 (2015).

Download references


We thank B. Deagle, S. D. Leaver, C. B. Lowe, S. D. Brady, J. Turner, K. Lindblad-Toh and the Broad Institute Genomics Platform for help with sequences, samples and morphometric analysis, and B. Moa for bioinformatics support. This work was funded by the National Research Council Canada grant NRC2354 to T.E.R. and National Institute of Health grants 3P50HG002568-09S1 ARRA and 3P50HG002568 to D.M.K.

Author information


  1. Department of Biology, University of Victoria, Victoria, British Columbia, Canada

    • David A. Marques
    •  & Thomas E. Reimchen
  2. Aquatic Ecology & Evolution, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

    • David A. Marques
  3. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland

    • David A. Marques
  4. Department of Developmental Biology, HHMI and Stanford University School of Medicine, Stanford, CA, USA

    • Felicity C. Jones
    •  & David M. Kingsley
  5. Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany

    • Felicity C. Jones
  6. Earlham Institute, Norwich Research Park, Norwich, UK

    • Federica Di Palma
  7. Department of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    • Federica Di Palma


  1. Search for David A. Marques in:

  2. Search for Felicity C. Jones in:

  3. Search for Federica Di Palma in:

  4. Search for David M. Kingsley in:

  5. Search for Thomas E. Reimchen in:


T.E.R. conceived the study, ran the experiment, collected fish and ecological data in the field, and acquired morphological data. D.M.K., F.C.J. and F.D.P. generated sequencing data and genotype calls. D.A.M. designed and performed all subsequent analyses and wrote the manuscript with contributions from all co-authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to David A. Marques.

Supplementary information

  1. Supplementary Information

    Supplementary Results, Supplementary Figures and Supplementary Data

  2. Reporting Summary

  3. Supplementary Tables

    Supplementary Table 1: List of genomic outlier regions. Supplementary Table 2: List of QTL overlapping with outlier regions. Supplementary Table 3: List of candidate genes centred on selective sweep signatures in outlier regions. Supplementary Table 4: Genomic evolution in the 13 generation selection experiment and beyond.

About this article

Publication history